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Vassetzky et al. Mobile DNA (2021) 12:10 https://doi.org/10.1186/s13100-021-00238-y RESEARCH Open Access New Ther1-derived SINE Squam3 in scaled reptiles Nikita S. Vassetzky1,2* , Sergei A. Kosushkin2, Vitaly I. Korchagin1 and Alexey P. Ryskov1 Abstract Background: SINEs comprise a significant part of animal genomes and are used to study the evolution of diverse taxa. Despite significant advances in SINE studies in vertebrates and higher eukaryotes in general, their own evolution is poorly understood. Results: We have discovered and described in detail a new Squam3 SINE specific for scaled reptiles (Squamata). The subfamilies of this SINE demonstrate different distribution in the genomes of squamates, which together with the data on similar SINEs in the tuatara allowed us to propose a scenario of their evolution in the context of reptilian evolution. Conclusions: Ancestral SINEs preserved in small numbers in most genomes can give rise to taxa-specific SINE families. Analysis of this aspect of SINEs can shed light on the history and mechanisms of SINE variation in reptilian genomes. Keywords: SINEs, Retrotransposons, Squamata, Reptilia, Evolution Background sequences recognized by the enzymes of their partner Genomes are invaded by various repetitive elements, the LINE for reverse transcription/integration. most abundant of which (at least in higher eukaryotes) A typical SINE consists of the head derived from one are Long and Short INterspersed Elements (LINEs and of the cellular RNA species (tRNA, 7SL RNA, or 5S SINEs, respectively). The amplification cycle of these ret- RNA); the body, the terminal part of which is recognized rotransposons includes the transcription of their gen- by the partner reverse transcriptase (RT); and the tail, a omic copies, reverse transcription and integration into stretch of simple repeats. There are variations; certain the genome. LINEs rely on the transcription by the cel- SINEs have no body or their body contains sequences of lular RNA polymerase II, while reverse transcription and unknown origin and function (some of them called cen- integration are fulfilled by their own enzymes. SINEs do tral domains) that are shared between otherwise unre- not encode any enzymes and employ the cell machinery lated SINE families, etc. [1]. for their transcription by RNA polymerase III (pol III) LINEs are found in the genomes of all higher eukary- and the machinery of their partner LINE for their reverse otes. Clearly, SINEs cannot exist without LINEs but not transcription and integration into chromosomes. Accord- vice versa; there are rare genomes that have LINEs but ingly, SINEs have pol III promoters for transcription and lack SINEs (e.g., Saccharomyces or Drosophila). During evolution, LINE (sub)families can become inactive and their partner SINEs also cease to amplify. If another * Correspondence: [email protected] LINE family becomes active in a particular genome, re- 1Institute of Gene Biology, Russian Academy of Sciences, Moscow 119334, placement of the sequence recognized by its RT can re- Russia animate a SINE [2]. Usually, a genome harbors one or 2Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, Moscow 119991, Russia several SINE families; some of them can be inactive and © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Vassetzky et al. Mobile DNA (2021) 12:10 Page 2 of 10 were amplified in the ancestors. The analysis of SINE found beyond Squamata (see below). The analysis of variation in different taxa allows us to use them as their consensus sequences has revealed three major reliable phylogenetic markers [3, 4]. subfamilies that we called Squam3A, Squam3B, and The main lineages of the reptile-bird clade are scaled Squam3C. reptiles (Squamata), tuatara (Rhynchocephalia), turtles (Testudines), crocodiles (Crocodilia), and birds (Aves). Squam3 structure Squamata, the largest order of reptiles, include the fol- Squam3 is a typical SINE [13] composed of the tRNA- lowing major lineages: Serpentes (snakes), Iguania (in- derived head, the body with a central domain and the cluding iguanids, agamids, chameleons), Anguimorpha, 3′-terminus matching that of the partner LINE, and the Scincomorpha, Lacertoidea, Gekkota, and Amphisbaenia. tail, a stretch of several simple repeats. The consensus Phylogenetic relations among squamate reptiles are sequences range from 218 to 239 nt (without tail). There highly controversial due to the conflicting signals pro- is no clear preference for a particular tRNA species vided by molecular, morphological, and paleontological (which is not uncommon among SINEs). data. Together with tuatara, the only extant representa- The body is similar to a fragment of the CORE central tive species of Rhynchocephalia, they form monophyletic domain; the pronounced similarity spans over 28 nt superorder Lepidosauria, which is the sister group to (double-overlined in Fig. 1). There is also a similarity Archelosauria, the clade that contains archosaurs (croco- with the very 3′-terminus of LINEs of the L2 clade iden- diles and birds) and turtles [5]. tified in Darevskia valentini (data not shown) and a less The first reptile SINE was found in 1990 in the pronounced similarity with L2 LINEs of Anolis caroli- Chinesepondturtle[6]; currently, we know approxi- nensis (L2-26_ACar and L2-24_ACar in Repbase). mately ten SINE families in reptiles [1] with a differ- The tail of Squam3 is largely composed of (TAAA)n or ent taxonomic distribution, e.g., Cry is limited to (CTT)n; however, certain species have (GTT)n, (ATT)n, turtles and degraded copies of AmnSINE, which was or poly(A) (Table 1). Squam3 has a very low rate of tar- active in the ancestor of amniotes [7], can be found get site duplications. This is unusual but not exceptional far beyond reptiles. Another example is Ther1 initially among SINEs and can point to an alternative cleavage described as a mammalian SINE (MIR) but renamed pattern in different DNA strands by the partner LINE later [8, 9]. Several known Ther1/MIR subfamilies endonuclease [13]. (MIRb, MIRc, and MIR_Testu) have minor differences from Ther1 except the Alligator mississippiensis’s MIR1_ Squam3 subfamilies AMi with an extended deletion. Moreover, active Ther1/ Genomic copies of SINEs are subject to random muta- MIR SINEs were found in non-avian reptiles, so ample tions; accordingly, single-nucleotide mutations can be and diverse derived SINEs could be expected in their ge- used to identify subfamilies only for highly conserved nomes [10]. This is further corroborated by active diversi- SINEs. We use extended insertions/deletions to distin- fication of reptilian L2 [11]. guish between the three major Squam3 subfamilies des- Despite active sequencing of genomes of various ignated as Squam3A, Squam3B, and Squam3C (Fig. 1). species of lizards and snakes, no detailed comparative Squam3B has a characteristic 11-nt insertion (marked in genomicstudiesofaSINEfamilyindifferenttaxaat pink in Fig. 1), and Squam3C has a characteristic 7-nt the order level are available. We discovered a new insertion (marked in blue in Fig. 1). There are also SINE named Squam3 in the genomes of Darevskia minor differences between the Squam3 subfamilies. In and Anolis lizards. Further analysis demonstrated their addition, there are sub-subfamilies; one of these distribution throughout squamates; a similar SINE (Squam3B3) has become a major variant in the two was found in the tuatara [12]butnotinotherreptiles Gekkonidae species. or birds. However, Squam3 remained unnoticed in al- Further analysis of Squam3-related sequences in the most 40 genomes of squamates. Here, we analyzed tuatara genome has revealed a similar SINE (tuaMIRa) the structure, distribution, and evolution of Squam3 with a 32-nt insertion (marked in amaranth in Fig. 1). and its relatives. This insertion restores the CORE central domain and makes the element similar to Ther1 (MIR). It should be Results noted that this deletion in Squam3 and tuaMIRс relative Squam3 identification to Ther1 is distinct from the deletion in MIR1_AMi The consensus sequence of Darevskia Squam3 was used (Fig. S2A). TuaMIR SINEs also have an 8–13-nt deletion to search the genomes of scaled reptiles. It was found in in the LINE-derived region (marked in violet in Fig. 1). all sequenced genomes (as well as in a variety of Gen- Moreover, another element (tuaMIRb) with a similar in- Bank sequences of squamate species whose genomes sertion lacks the ~ 40-nt region between the CORE and have not been sequenced; Table S1). No Squam3 was the LINE-derived region conserved in other Squam3- Vassetzky et al. Mobile DNA (2021) 12:10 Page 3 of 10 Fig. 1 Sequence alignment of Squam3 subfamilies of squamate reptiles with tuatara tuaMIR SINEs and Ther1. The tRNA-derived region, CORE central domain, LINE-derived region, and tail are indicated above the sequences. See text for other explanations and Ther1-related SINEs but has a much longer L2 reported these SINEs, so we use their nomenclature of LINE-derived region due to the 77-nt insertion (marked tuatara SINEs.

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